Root lesion nematode (P. penetrans).

Root lesion nematodes (Pratylenchus spp.) are globally widespread plant parasites that affect many crops. In a 2012 survey (Jones et al. 2013), these nematodes were voted as the third most economically important group of nematodes. They are polyphagous, migratory endoparasites found near and in roots of plants (Fig. 3A and B). As their name suggests, feeding on roots creates lesions and necrotic areas, resulting in reduced root growth and even plant death. Severe feeding affects aboveground biomass, reducing growth and crop yield (Fig. 3C and D). Their migratory nature and lack of obvious feeding patterns make them a challenging pathogen to investigate (Castillo and Volvas 2007; Jones and Fosu-Nyarko 2014).

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Pratylenchus penetrans parasitizes more than 400 plant species, including red raspberry (Castillo and Volvas 2007; Rudolph and DeVetter 2015; Zasada et al. 2015). This nematode is of special importance for red raspberry in the PNW because of the limited environmental range suitable for red raspberry production (Rudolph and DeVetter 2015) and because raspberry-grower profit margins are narrow (Walters et al. 2017), making economical and sustainable control methods critical for growers. This pest also affects red raspberry production significantly in Scotland and other parts of Europe (Hall et al. 2009).

Historically, fenamiphos and methyl bromide were important nematicides used in the United States to control this pest. As environmental standards and policies have tightened, approved fumigants have become fewer and more difficult to use, reducing grower access to effective chemical treatments for nematodes (US Environmental Protection Agency 2008; Zasada et al. 2010). The raspberry industry in the PNW relies heavily on soil fumigation and primarily uses 1,3-dichlorpropene for preplant fumigation to reduce nematode densities, primarily focused on P. penetrans (Zasada et al. 2010). Investigations into nonchemical strategies to manage P. penetrans have included brassicaceous seed meal, compost, mulch, root removal, solarization, cover crops, and crop rotation (DeVetter et al. 2018; Forge and Kempler 2009; Forge et al. 2012, 2014, 2016; Gigot et al. 2013; Pinkerton et al. 2000, 2009; Rudolph et al. 2017, 2018, 2019b; Trudgill and Brown 1992; Vrain et al. 1996; Walters et al. 2017; Zasada et al. 2009). Most of these strategies were not found to be comparably effective compared with soil fumigation, or were uneconomical for the grower, leaving preplant soil fumigation as the primary industry method for nematode management. Available fumigant treatments can reduce nematode densities, but the nematode is never eliminated from a field.

Raspberry bushy dwarf virus.

RBDV is a pollen-borne viral disease that is characterized by poor drupelet set and crumbly fruit in some infected plants, and is accentuated by coinfections with Raspberry leaf mottle virus (RLMV) and Raspberry latent virus (RpLV) (Martin et al. 2013; Quito-Avila et al. 2014). RBDV resistance is a major objective in raspberry breeding programs. Although commercial cultivars are often symptomless when infected only with RBDV, the namesake dwarf phenotype arises when coinfections with Black raspberry necrosis virus (BRNV) occur (Jones 1979). Fruit from infected plants is susceptible to crumbling resulting from weak drupelet set or drupelet abortion (Murant et al. 1974). As a result, fruit may be rejected from the high-value individual quick-frozen market by processors, forcing growers to sell their fruit into lower grade juice, jam, or crumbled fruit markets (Washington Red Raspberry Commission, unpublished information). Losses from poor fruit set caused by RBDV are estimated to be as high as $2470/ha per year (Moore and Martin 2008).

RBDV was originally classified among the tripartite ilarviruses of the family Bromoviridae before being classified into a new genus Idaeovirus within Bromoviridae and was most recently placed into the family Mayoviridae because of its genomic properties (Martin and Keller 2021; Ziegler et al. 1992, 1993). Isometric virions are ∼33 nm in diameter and are composed of a single-stranded RNA bipartite genome with RNA-1, RNA-2, and RNA-3 (Barnett and Murant 1970; Mayo et al. 1991; Natsuaki et al. 1991; Ziegler et al. 1992). RNA-1 is 5449 nucleotides and RNA-2 is 2231 nucleotides; both are genomic RNA. RNA-3 is 946 nucleotides and has been classified as a subgenomic monocistronic coat protein messenger RNA derived from RNA-2. To date, RBDV remains the only officially accepted species in the Idaeovirus genus (International Committee on Taxonomy of Viruses 2011). While predominantly a concern in Rubus, plants in the families Amaranthaceae, Chenopodiaceae, Cucurbitaceae, Leguminosae, and Solanaceae were also hosts after manual sap inoculation, but the virus did not readily spread from Rubus to these plants (Barnett and Murant 1970). RBDV was graft transmissible in other Rosaceae species such as quince (Cydonia oblonga), the hybrid Pyronia veitchii, and alpine strawberry (Fragaria vesca) (Credi et al. 1986; Jones et al. 1982). The first report of a natural infection of RBDV outside of raspberry was in grape (Vitis vinifera) in Slovenia and later also in Serbia, but has since been reported in sweet cherry (Prunus avium) in Turkey (Çağlayan et al. 2023; Jevremović and Paunović 2011; Mavrič et al. 2003; Mavrič Pleško et al. 2009).

A significant challenge in breeding for RBDV resistance is the nature of transmission. The pollen-borne virus is transmitted horizontally and vertically, resulting in infections of nearby plants and resulting seed (Barnett and Murant 1970; Cadman 1965; Murant et al. 1974). Because raspberries rely on insect pollinators, this appears to contribute to horizontal transmission, but there are no known insect vectors (Bulger et al. 1990; Murant et al. 1974). A needle nematode, Longidorus juvenilis, was reported to be positive for RBDV; the vector status of this nematode is still being investigated (Mavrič Pleško et al. 2009). Insecticides do not appear to reduce viral spread. Current management recommendations are to cultivate virus-free plants away from wild Rubus stands such as thimbleberry (R. parviflorus), which can harbor the virus. Growing virus-infected plants appeared to contribute to viral spread more than field proximity to wild stands (Špak and Kubelková 2000). However, eliminating RBDV from infected plants for continued use as parents and selections in breeding is difficult and time-consuming, even with the aid of tissue culture and thermotherapy (Chambers 1961; Lankes 1995; Mathew et al. 2021; Theiler-Hedtrich and Baumann 1989). For these reasons, RBDV is a major challenge not only in grower fields, but also for nursery propagation and maintenance of virus-free breeding populations.

Phytophthora root rot (P. rubi).

Phytophthora rubi [Wilcox and Duncan (Man in’t Veld 2007)] is an economically significant soilborne pathogen of red raspberry commonly found in Washington, USA; British Columbia, Canada; and the northeastern United States (Gigot et al. 2013; Sapkota et al. 2022; Stewart et al. 2014; Weiland et al. 2018; Wilcox 1989). Black raspberries may also be infected but are generally much less susceptible (Fiola and Swartz 1994; Funt 2013; Wilcox and Cooke 2017). In addition to P. rubi, other Phytophthora species, such as P. cactorum and P. megasperma, may be important locally or regionally (Montgomerie and Kennedy 1980; Weiland et al. 2024; Wilcox 1989). Phytophthora rubi often co-occurs with other soilborne pathogens, including P. penetrans, V. dahliae, and various other Fusarium, Cylindrocarpon, Rhizoctonia, and Pythium species (Gigot et al. 2013; Weiland et al. 2018). Together, these pathogens are suspected of forming a soilborne disease complex that contributes to an overall decline in raspberry health, productivity, and field longevity (Weiland et al. 2018). However, P. rubi appears to be among the most damaging of the soilborne pathogens, and fields where P. rubi occurred were more than twice as likely to have severe root rot symptoms than fields where it did not occur.

Phytophthora species are not true fungi, but are more closely related to brown algae, and are properly classified as oomycetes (water molds). Oomycetes produce motile spores (zoospores) in response to high soil moisture. Zoospores are attracted to root exudates, and swim to fine roots where they initiate infection. Excessive irrigation, precipitation, or poor drainage can exacerbate infection and lead to significant plant loss (Duncan and Kennedy 1989; Wilcox and Cooke 2017). Phytophthora rubi zoospores are likely produced in late spring and summer, when field soils are warm, near 21 °C (Graham et al. 2021). Most Phytophthora species also produce thick-walled survival spores (either chlamydospores or oospores), which can survive for years in the soil. Combined, these characteristics can cause root rot to develop very rapidly when conditions are optimal, and make the pathogen extremely difficult to control in infested fields.

Once infection has occurred, P. rubi rots the fine roots, leaving larger structural roots behind. Lesions may develop on large roots and extend above the soil line into the lower cane, which may shrivel and turn reddish brown to purple or black (Stewart et al. 2014; Weiland et al. 2018; Wilcox and Cooke 2017). Scraping away the bark reveals water-soaked, reddish brown lesions with a distinct margin between recently killed and healthy tissues (Fig. 4A). Injured roots become increasingly unable to transport water and nutrients, leading to aboveground symptoms of stunting, wilting, leaf chlorosis or reddening, and cane death (Fig. 4A and B). These symptoms may occur on only one or two canes, or may affect the entire plant. Severe infections can cause up to 100% plant mortality in grower fields (Gigot et al. 2013; Weiland et al. 2018).

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In the PNW, a combination of preplant soil fumigation, raised beds, resistant cultivars, and fungicides are used to manage P. rubi. Several fungicides are available and effective, including mefenoxam, phosphorous acid, and oxathiapiprolin (Heiberg 1995, 1999; Sapkota et al. 2023a, 2023b; Weiland et al. 2024; Wilcox et al. 1999). Amendments such as gypsum have been investigated and have shown promising results as part of a successful integrated pest management plan in conjunction with raised beds, resistant cultivars, solarization, and chemical controls (Maloney et al. 1993, 2005; McGregor and Franz 2002; Pinkerton et al. 2009). Biological controls have also been investigated in vitro but have not yet been examined under field conditions (Toussaint et al. 1997; Valois et al. 1996).

Verticillium wilt (V. dahliae).

Although P. rubi is the most destructive root pathogen of red raspberry, V. dahliae is the most damaging root and vascular pathogen of black raspberry (Mercier and Kong 2017). Unlike P. rubi, V. dahliae is a true fungus. It can survive in field soil for decades as hard, microscopic structures called microsclerotia. Microsclerotia germinate in response to root exudates and infect the fine roots of susceptible plant hosts. Once infection has occurred, the pathogen plugs and kills the water-conducting tissues (xylem), leading to wilting and cane death (Fig. 5). Unlike Phytophthora species, V. dahliae does not cause root decay, thus the fine root system may still be intact on recently killed plants. Infected canes may be discolored purple to black and are very similar in appearance to canes killed by P. rubi. Therefore, plant samples should be sent to a diagnostic laboratory to confirm which pathogen is present, because many fungicides used to manage P. rubi are ineffective against V. dahliae.

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Although red raspberry is not as susceptible to V. dahliae as black raspberry, severe infection is observed occasionally, especially when caneberries are grown in fields that were cropped previously with potato (Solanum tuberosum) or mint (Mentha spp.) (Weiland et al. 2018). Both mint and potato are highly susceptible to V. dahliae, and cropping with either of these plants can cause soil populations of the pathogen to build up to extremely damaging levels, resulting in major damage on caneberries grown in the field afterward.

Verticillium wilt is extremely difficult to manage once a field becomes infested. In woody crops, the disease is most commonly managed by either not planting susceptible crop species into fields where the pathogen is present or by preplant fumigation under tarp (Mercier and Kong 2017). This is a challenge in Oregon, where black raspberry is commonly planted in fields that previously contained other host crops such as potato. Unfortunately, there are no known fungicides that are effective against this disease. Solarization can reduce soil populations of the pathogen (Pinkerton et al. 2000), but the effect is inconsistent and does not penetrate deeply enough into the soil profile to provide effective, long-lasting disease control in northern locations. Host resistance has not been well explored in black raspberry cultivars, although hybrids containing red raspberry parentage were more tolerant of Verticillium wilt than those containing only black raspberry parentage (Fiola and Swartz 1994). Similarly, only one or two of 17 black raspberry accessions had low symptom severity after inoculation in a greenhouse screening assay, although this effect was intermittent and severe disease was occasionally seen on all 17 genotypes (Weiland JE, unpublished data).

Gray mold (B. cinerea).

Botrytis cinerea is a necrotrophic, haploid, ascomycete fungus that affects more than 1400 plant species worldwide (Alfonso et al. 2000; Fillinger 2016; Garfinkel et al. 2019; Ma and Michailides 2005; Staats et al. 2005; Williamson et al. 2007). Botrytis cinerea is the causal agent of cane blights, rots, and gray mold, a globally destructive disease that causes significant yield loss of red raspberry in the field and postharvest (Elad et al. 2004; Leroux 2007). The regional climate in the PNW contributes to high disease pressure from Botrytis spp. on red raspberry. Botrytis spp. can infect any foliar part of the plant, particularly leaves, buds, flowers, or fruit at a variety of developmental stages (Fig. 6) (Williamson et al. 2007). Infection of raspberry flowers and berries reduced yield and berry quality directly (Dashwood and Fox 1988; Kozhar and Peever 2018). The global annual cost to control B. cinerea exceeds $1 billion/year and management relies heavily on the use of synthetic fungicides (Leroux 2007; Yin et al. 2012).

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Botrytis cinerea is a high-risk fungal pathogen for the development of fungicide resistance as a result of its rapid life cycle, genetic diversity, and high fecundity (Atwell et al. 2015; Hahn 2014). Resistance to Fungicide Resistance Action Committee (FRAC) classes, including demethylation inhibitors, succinate dehydrogenase inhibitors, and quinone outside inhibitors has been reported worldwide (Hahn 2014; Zhang et al. 2016) and is a serious limitation for effective disease control. In the PNW, the primary management strategy for gray mold has been the use of fungicides with single-site modes of action (Hahn 2014). Growers often alternate fungicides with different FRAC codes, determined by their modes of action, to slow the development of resistance (Konstantinou et al. 2015; Polat et al. 2018; Zhang et al. 2016).

Further investigations have revealed there are genetic differences in B. cinerea populations with regard to fungicide sensitivities (Fournier et al. 2002; Konstantinou et al. 2015; Leroux et al. 2002; Martinez et al. 2005; Martínez et al. 2008). Differences in fungicide resistance profiles could be related to high levels of genetic diversity and restricted gene flow among the different cryptic groups of B. cinerea (Fournier et al. 2002, 2005; Giraud et al. 1997; Leroux et al. 2002; Martinez et al. 2003; Martínez et al. 2008; Walker et al. 2011). Fournier and Giraud (2008) demonstrated high Botrytis spp. genetic diversity within fields. Hu et al. (2018) showed a high diversity between isolates from the same location, and even on the same host plant, with multiple haplotypes exhibiting different fungicide-resistant profiles existing on the same plant tissue. The high genetic diversity of these pathogens and lack of clear genetic resistance in commercially elite germplasm make it a challenge to address by breeding efforts.

Spotted-wing Drosophila (D. suzukii).

Originating in east Asia, SWD (syn. Asian vinegar fly; D. suzukii) has become one of the most important insect biotic stresses for small fruits and stone fruits such as blueberry, caneberries, strawberry, and cherry within the past two decades (Lee et al. 2011). It was introduced to the continental United States in California in 2008, and by 2015, was present in most states (Asplen et al. 2015). Compared with other fruit, red raspberry is a preferred host for SWD (Bellamy et al. 2013; Burrack et al. 2013).

This fly has a serrated ovipositor that allows it to penetrate the fruit skin and lay eggs within ripening fruit (Fig. 7A). The developing larvae feed on the fruit tissue, inflicting heavy damage. The infested fruit is subject to rejection by fruit packers, sellers, and importers because of the presence of SWD, infections from other pathogens resulting from SWD damage, and violations of maximum residue limits from pesticide applications (Goodhue et al. 2011). In California, crop damage from SWD can lead to temporary price increases for growers, but overall represents significant revenue reductions (Goodhue et al. 2011).

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Since its introduction, there has been heavy reliance on insecticides to manage SWD, but in recent years there has been emerging research demonstrating the use of biological control agents (e.g., parasitoid wasps, insect and avian predators, entomopathogenic nematodes), nonhazardous sugar substitutes (e.g., erythritol), and physical barriers and deterrents (e.g., exclusion netting, plastic mulch) for management (Carroll et al. 2023; Choi et al. 2017; Lee et al. 2019; McIntosh et al. 2023; Sampson et al. 2017; Stockton et al. 2020). Since 2022, releases of the imported parasitoid Ganaspis kimorum have been made throughout the United States, and another parasitoid originally from Asia, Leptopilina japonica, has established on its own throughout North America (Gariepy et al. 2024). The impacts of these parasitoids on SWD populations are being monitored.

American large raspberry aphid (A. agathonica).

The large raspberry aphid (syn. raspberry aphid, common raspberry aphid) is a significant concern for red raspberry production in North America and Europe. The species differ between the two locations. The American large raspberry aphid is A. agathonica (Fig. 7B), whereas the European large raspberry aphid is A. idaei.

Feeding on raspberry plants by the American large raspberry aphid can result in leaf curl, which on its own is not detrimental to the plant (Funt 2013). The detrimental effect is the aphid’s role as a vector for many of the viruses that contribute to the raspberry mosaic virus complex and the raspberry crumbly fruit complex. The raspberry mosaic virus complex includes BRNV, RLMV, and Rubus yellow net virus (RYNV) (Martin et al. 2013). The raspberry crumbly fruit complex is comprised of RBDV, RLMV, RYNV, and RpLV (Martin et al. 2013). Of all these viruses, RBDV is the only one that is not transmitted by aphids (refer to earlier section). To add to this complexity, each of these viruses are transmitted in variable manners, with BRNV transmitted nonpersistently, RYNV and RLMV likely transmitted semipersistently, and RpLV transmitted persistently (Cadman 1954; Halgren et al. 2007; Jones et al. 2002; Quito-Avila et al. 2012).

Options for aphid management include biocontrols (e.g., parasitic wasps), cultural controls (e.g., removal of plant debris), chemical controls (e.g., imidacloprid), and plant genetic resistance. No genes have been identified that confer resistance to these viruses, and research has therefore focused on improving resistance to the insects that transmit virus.

Rose stem girdler (A. cuprescens).

Since 2022, the rose stem girdler has been found from the southern Willamette Valley of Oregon, USA, to the Canadian border of western Washington, USA (O’Dea 2024). Introduced from Europe, it was first reported in the eastern United States as early as 1913.

The insect is a metallic-colored beetle that lays its eggs on the canes of various Rubus species and rose plants (Fig. 7C). The hatched larvae tunnel and feed inside the cane that girdles the canes. Girdling can cause galling in first-year canes, can increase cane snapping and breakage significantly, and can reduce fruit production in second-year canes. Heavy infestation for 2 to 3 years will kill plants. The larvae overwinter inside the canes and emerge as adults from late May to early June after accumulating ∼900 h at more than 55 °F (O’Dea and Hill 2022).

Effective monitoring with traps for the rose stem girdler is still in need of development. Currently, growers are recommended to use insecticides for 3 weeks after pest emergence, and to prune canes with damage. Pruned canes need to be removed or destroyed to kill the overwintering larvae. A parasitoid that attacks the larval stage, Baryscapus rugglesi, has been found regularly in the PNW (O’Dea et al. 2023). Because this parasitoid is already naturally occurring, a greater understanding of conservation practices to enhance its effectiveness is needed.

Genetics of root lesion nematode resistance.

Bristow et al. (1980) evaluated the reaction of 18 red raspberry cultivars to P. penetrans and found that some cultivars showed heavy infestations by P. penetrans, but with no significant impact on biomass fresh weight compared with the controls. This suggested that the raspberries under investigation possessed varying degrees of tolerance to P. penetrans; however, the authors speculated that the method used may not have elicited a significant response from the plants. Vrain and Daubeny (1986) performed a similar experiment with 21 red raspberry genotypes, including 10 from the experiment by Bristow et al. (1980) and four related Rubus cultivars. Some cultivars demonstrated tolerance, and some demonstrated resistance based on the number of nematodes present and effects on plant growth and development, perhaps indicating that tolerance may be sustained for some time before a plant shows symptoms of P. penetrans parasitism. More recently, Zasada and Moore (2014) evaluated the reaction of a panel of Rubus species to P. penetrans in a greenhouse trial, including some of those from the Vrain and Daubeny (1986). The host status of R. crataegifolius ‘Jokgal’ was inconclusive in this trial, although Vrain and Daubeny (1986) previously found ‘Jokgal’ to support low densities of P. penetrans. Zasada and Moore (2014) observed that two black raspberry species, R. niveus and Rubus leucodermis, were poor hosts for P. penetrans across years and that they may be useful in breeding programs. However, raspberry ‘Tulameen’ (PI 618441) (Daubeny and Anderson 1991), which has R. niveus in its pedigree, did not support lower P. penetrans densities consistently compared with the industry standard ‘Meeker’.

Current information on the host status of various clones and insights into the genetics of P. penetrans resistance suggest that P. penetrans resistance is quantitative and influenced by genetic background. Vrain et al. (1994) further investigated the mode of inheritance for P. penetrans resistance using a half-diallel analysis with crosses between two resistant and two susceptible genotypes. Resistance of red raspberry to P. penetrans was determined to be a quantitative trait, as no bimodal distributions indicative of a qualitative trait were observed for the recorded traits. A limitation of that study was its small sample size. Larger family size may reduce variability and allow determination of the resistance inheritance mode. To date, no published studies have evaluated and characterized P. penetrans resistance using genomic or quantitative genetic approaches.

Genetics of RBDV resistance.

A single resistance gene to RBDV known as Bu was identified in the early 1980s (Jones et al. 1982; Murant et al. 1982). This is a dominant gene that appears to confer complete immunity to Scottish or common RBDV isolates (RBDV-S). Resistant cultivars possessing Bu are heterozygous. Cultivars homozygous for Bu were not identified, suggesting that the homozygous state may be deleterious to plant health or is in linkage with other deleterious alleles (Stephens et al. 2016). Since the discovery of the Bu gene, there have been intensive efforts to incorporate this gene while maintaining other desirable traits. Stephens et al. (2016) located potential markers for use in marker-assisted selection (MAS), as did Ward et al. (2012). However, marker accuracy was dependent on pedigree, and additional work is needed to determine marker usefulness for breeding. Genetic engineering has also been explored as an avenue for RBDV resistance. Red raspberry ‘Meeker’ was transformed successfully with the coat and movement protein genes of RBDV using Agrobacterium-mediated transformation to confer resistance to the common RBDV isolates (Martin and Mathews 2001; Martin et al. 2001). However, public wariness and governmental regulations of transgenic plants have impeded the advancement of these plants for cultivation or use as parents for breeding resistant progeny.

After the identification of Bu, resistance-breaking isolates were discovered in 1981 in the United Kingdom at about the same time that seed from the former Union of Soviet Socialist Republics was introduced to the area (Barbara et al. 1984; Knight and Barbara 1981; Murant et al. 1982). Identifying additional sources of resistance became very important. Previous studies indicated the presence of additional resistance genes that were never fully identified, but which appeared to provide quantitative resistance to the resistance-breaking isolate when Bu was also present (Jennings and Jones 1989; Jones et al. 1982). Although resistance-breaking isolates have been observed in the United Kingdom and other European countries, the first report in the United States came from Washington in 2014 (Lanning 2014; Lanning et al. 2016). A viral survey would be of great benefit to researchers and breeders as there have not been any further reports of this strain in the United States.

Genetics of Phytophthora root rot resistance.

Identifying and understanding Phytophthora root rot has been a significant goal of breeding programs in the PNW since the 1970s, and in the United Kingdom since the 1980s (Barritt et al. 1979, 1981; Knight et al. 1989). Barritt et al. (1979) screened germplasm for resistance or susceptibility to Phytophthora root rot and determined high heritability estimates for resistance, concluding that resistance was additive, and rapid genetic gain was achievable. Knight and Fernández-Fernández (2008) evaluated the nature of resistance in a half-diallel analysis and suggested that resistance was an additive, quantitative trait. Similar results were obtained by Nestby and Heiberg (1995); however, they found that nonadditive gene action occurred as well.

As molecular techniques have advanced, our understanding of the underlying genetic mechanisms and modes of inheritance for Phytophthora root rot resistance has improved and reinforced some of the conclusions of past studies. Like Nestby and Heiberg (1995), Pattison et al. (2007) demonstrated multiple gene actions. Depending on the trait being measured (petiole lesion incidence and plant disease index), additive or dominance effects may have accounted for a significant proportion of the variance. Their results suggested other gene effects contributed to recorded phenotypes alongside additive and/or dominance effects, and Pattison et al. (2007) proposed that qualitative or quantitative measures could be used to evaluate and improve resistance. The application of molecular markers for selecting resistant genotypes was demonstrated by Weber et al. (2008), who found that a sequence characterized amplified region marker and a cleaved amplified polymorphic sequence marker were 62% and 56% accurate, respectively, in selecting a resistant individual. Use of both markers allowed for the retention of 85% of resistant individuals. Additional quantitative trait loci (QTLs) associated with Phytophthora root rot resistance allowed for further investigation into potential mechanisms of resistance, such as the involvement of auxin or germin-like protein in the initiation of new axial growth as a defense response. These QTLs can support the development of predictive molecular marker assays to increase selection efficiency for resistant raspberry progeny using MAS (Graham et al. 2011; Pattison et al. 2007).

Several available red raspberry cultivars have desirable levels of Phytophthora root rot resistance, including ‘Latham’ and ‘Asker’. In addition, wild, uncultivated species have been examined as novel sources of genetic resistance for root rot (Barritt et al. 1979; Røen et al. 2012). Several of these species possess desirable resistance levels, such as R. spectabilis, as well as R. coreanus, R. inominatus, R. niveus, R. lasiostylus, and R. strigosus (Kempler et al. 2012; Knight 1991). Breeding efforts by the WSU raspberry breeding program for improving red raspberry resistance to Phytophthora root rot has produced several notable red raspberry cultivars from the ‘Cascade’ series with moderate to high levels of resistance, including ‘Cascade Delight’, ‘Cascade Harvest’, ‘Cascade Bounty’, and ‘Cascade Dawn’ (Moore 2004, 2006; Moore and Finn 2007; Moore et al. 2015).

Genetics of Verticillium wilt resistance.

Despite the importance of Verticillium wilt in black raspberry production, there are few publications elucidating resistance or sources of resistance. No resistance to Verticillium wilt has been reported for released black raspberry cultivars (Fiola and Swartz 1994; Zeller 1936). Resistance in red raspberry and blackberry has been established. Red raspberry cultivars such as ‘Antwerp’, ‘Cayuga’, ‘Cuthbert’, ‘Marlboro’, ‘Ohta’, ‘Owasco’, ‘Seneca’, ‘Superlative’, and ‘Syracuse’ can potentially serve as sources of resistance for black raspberry breeding (Darrow 1937). However, cultivars resistant to one strain of V. dahliae may not be resistant to others, as noted by Zeller (1936). Resistance and tolerance have been further demonstrated in Asiatic species of red raspberry (Zeller 1936). Native PNW species, R. spectabilis and R. parviflorus, had minimal to no symptoms of infection and serve as additional sources of resistance. Other regional species such as R. leucodermis are long-lived in the face of infection, but with significant yield losses.

Early breeding efforts indicated that the mechanisms of resistance may be quantitative. Backcrossing to red raspberry has not resulted in distinct segregating phenotypes. In addition, progeny in subsequent generations show weak or no resistance, suggesting that numerous small-effect genes may be at play (Keep 1976, 1989). A partial diallel analysis also indicated additive gene action and tolerance rather than resistance (Fiola and Swartz 1994). Verticillium dahliae was isolated from resistant cultivars, indicating these plants remained economically productive under infection (Fiola and Swartz 1994). More recently, an RNA sequencing study was performed to identify candidate genes involved in V. dahliae infection in black raspberry (Bushakra et al. 2016). Several transcripts were identified as homologs to the Ve1 resistance gene in tomato, but were not detected among the differentially expressed genes (DEGs) characterized in the study. Other general pest and pathogen response genes were observed among the DEGs. The identification of these genes in response to V. dahliae infection presents the opportunity to understand tolerance in black raspberry more fully.

Genetics of B. cinerea resistance.

The earliest publications from breeding programs detailed the struggle to develop cultivars with Botrytis resistance. One of the primary complications is that the same causal organism causes two diseases: cane Botrytis and gray mold (syn. fruit Botrytis). Cane Botrytis appears to be a significant contributor to gray mold development in fruit (Jennings and Brydon 1989). Knight (1980a) also found a positive correlation between cane Botrytis and gray mold incidence. Jennings and Carmichael (1975) recommended selecting individuals resistant to cane Botrytis and gray mold to reduce inoculum. In contrast, other researchers determined there was no strong correlation between cane Botrytis and gray mold development and stated that prior reports of significant correlations were the result of a few strong correlations in evaluated cultivars (Daubeny and Pepin 1981; Knight 1980b).

Decades of research by breeding programs in British Columbia, Scotland, and England indicate that cane Botrytis resistance is complex and is likely conferred by a combination of additive, minor genes and few major genes (Daubeny 1987; Jennings 1983; Jennings and Brydon 1989). Gene H, which is responsible for cane pubescence, also appeared to be associated significantly with cane Botrytis resistance (Graham et al. 2006), although not strongly (Knight 1980a). Whether this association was a result of linkage with resistance genes or physiological differences that deterred infection is unknown (Graham et al. 2006). Resistance not associated with gene H has been noted to be present in the Asiatic species R. pileatus, R. crataegifolius, R. coreanus, and Rubus mesogaeus and the North American species R. occidentalis and R. strigosus (Jennings 1983; Jennings and Brydon 1989; Jennings and Williamson 1982; Keep et al. 1977; Knight 1980a, 1980b). It is believed that red raspberry ‘Chief’ (PI 553508) inherited this resistance from the R. strigosus in its pedigree (Daubeny 1987).

Most of the published studies in postharvest fruit rot resistance date back at least 45 years. Resistance has been observed in R. occidentalis, R. crataegifolius, and Rubus phoenicolasisus (Kichina 1976; Knight 1980a, 1980b). Red raspberry ‘Matsqui’ (PI 553391) and ‘Cuthbert’ have repeatedly demonstrated low gray mold incidence in fruit rot testing procedures (Barritt 1971; Daubeny and Pepin 1969, 1974). Red raspberries ‘Carnival’ (PI 553481), ‘Meeker’, ‘Glen Isla’ (PI 553510), ‘Nootka’, and ‘Ottawa’ have also been reported to have low gray mold incidence (Barritt 1971; Daubeny and Pepin 1969, 1974). Combined, it appears that there is tolerance primarily occurring in the cultivars reported to have low disease incidence. Furthermore, there appears to be correlations in berry color and other characteristics to resistance, as Harshman et al. (2014) found purple and black raspberries resisted rot the longest. Resistant raspberries had the highest phenolics and anthocyanins and the lowest ethylene evolution rates, which may be contributing to delayed disease development. The researchers suggested that breeding for low ethylene production of berries may protect against rot.

Genetics of SWD resistance.

Host plant resistance is also critical in integrated pest management, although few studies related to SWD have occurred in red raspberry. Strong resistance against SWD has not been observed, but some cultivars are more susceptible to SWD than others (Burrack et al. 2013; Lee et al. 2011; Wöhner et al. 2021). Lee et al. (2011) found no difference in susceptibility to SWD for six cultivars (Table 2). Burrack et al. (2013) also evaluated several berry crops, including nine red raspberry cultivars (Table 2), against SWD and detected variable infestation rates but no resistance among cultivars. However, there was a need to validate the apparent reduced preference among cultivars, which had lower infestation rates (Burrack et al. 2013). Wöhner et al. (2021) evaluated 37 floricane and 23 primocane fruiting red raspberry cultivars and confirmed previous reports of varying levels of susceptibility and an absence of strong resistance to SWD. Of the 60 cultivars tested, only ‘Dorman Red’ (PI 553425), a Mississippian floricane fruiting type (Overcash 1972), and ‘Pokusa’, a Polish primocane fruiting type, were classified as tolerant. Infestation appeared to be strongly correlated to berry firmness, but was not correlated with Brix and acidity. This finding contrasts with previous reports of a positive correlation between Brix and SWD development, and a lack of correlation with pH (Lee et al. 2011). Many other cultivars have not been evaluated, and assessing common PNW raspberry cultivars for susceptibility to SWD would be useful.

Table 2. Red raspberry (Rubus idaeus) cultivars evaluated for spotted-wing drosophila (Drosophila suzukii) resistance.

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Genetics of American large raspberry aphid resistance.

Genetic resistance to A. agathonica has been studied since the 1920s to mitigate the spread of the raspberry mosaic virus complex (Rankin 1927; Rankin and Hockey 1922). Research has indicated separate resistance genes to A. idaei and A. agathonica, which were thought to be the same species before the discovery of these genes (Hill 1956).

To date, few known resistance genes to A. agathonica have been identified in raspberry. Resistance genes Ag₁, Ag₂, Ag₃, Ag₄, and Ag₅, and an undesignated resistance gene (syn. Ag₆) have been discovered in plants from the northeastern United States or southeastern Canada (Daubeny 1966; Daubeny and Stary 1982; Dossett and Finn 2010). In contrast, 13 resistance genes to A. idaei are known in Europe (A₁–A₁₀, A_K4a, A_L518, and A_cor) (Fernández-Fernández et al. 2013; Knight et al. 1959, 1960; Ourecky 1975). The most well-known and deployed resistance gene, Ag₁, was originally found in red raspberry ‘Lloyd George’ and was used for more than 50 years in breeding programs (Daubeny 1966). However, an aphid biotype was discovered in the early 1990s that broke resistance conferred by Ag₁ (Daubeny and Anderson 1993). Ag₂ and Ag₃ are also dominant genes derived from red raspberry, specifically a wild R. strigosus population found in Ottawa, Canada, but unlike Ag₁, these genes were complementary and conferred only partial resistance (Daubeny and Stary 1982). The phenotypic similarities between the three genes has made it challenging to incorporate Ag₂ and Ag₃ reliably into new red raspberry cultivars (Dossett and Kempler 2012). Ag₄, Ag₅, and Ag₆ resistance genes come from R. occidentalis accessions collected from Maine and Michigan, USA, and Ontario, Canada. These three genes are of great interest because native genes are easier to integrate into breeding lines than red raspberry resistance genes. Introgression from red raspberry involves several generations of backcrossing to reconstitute the black raspberry fruit phenotype from the “purple hybrids” that result from black raspberry and red raspberry crosses (Dossett and Finn 2010). Ag₆ had similar phenotypic responses as Ag₄ and requires further investigation to determine its novelty (Dossett and Finn 2010).

Wild R. strigosus accessions have been of significant interest because these plants have demonstrated resistance to the aphid and are the source of Phytophthora root rot resistance in red raspberry cultivars such as ‘Newburgh’ and ‘Latham’ (Daubeny and Stary 1982; Daubeny et al. 1992). Accessions of R. idaeus, R. spectabilis, R. crataegifolius, and R. parviflorus also have aphid resistance (Daubeny et al. 1992). The details of these resistance sources remain vague and have not yet been compared with previously identified resistance genes. Although these sources may have underutilized resistance, incorporating these genetics presents additional challenges, including limited diversity, varying degrees of hybrid compatibility with R. idaeus or R. occidentalis, and the incorporation of undesirable wild traits following successful interspecific hybridization.

Additional research into the resistance mechanisms of these genes may aid breeding efforts. Aphid resistance has been characterized as either antixenosis resistance (affects feeding and alters insect behavior), antibiosis resistance (affects biotic potential of the insect such as fecundity)or tolerance (the plant’s ability to remain economically vigorous in the face of infestation) (van Emden 2007). To date, Ag₁, Ag₄, Ag₅, and an undesignated resistance gene have been evaluated for their resistance mechanisms. Ag₁ demonstrated antixenosis, as did Ag₄ to Ag₆, making it difficult to distinguish each of these genes based on phenotype alone (Kennedy and Schaefers 1974; Lightle et al. 2012, 2015). Although still unclear, Ag₂ and Ag₃ may have more of an antibiotic mechanism, as small colonies of aphids were observed on these plants (Daubeny and Stary 1982). Similar observations of red raspberry ‘Washington’ were made by Kennedy and Schaefers (1974), who concluded that ‘Washington’ demonstrated antibiosis. ‘Washington’ is derived from a cross between ‘Cuthbert’, a chance seedling selected from the wild in the northeastern United States, likely derived from R. strigosus, and ‘Lloyd George’, a chance seedling selected from the wild in Scotland, likely derived from R. idaeus. It appears that ‘Washington’ did not inherit Ag₁ from ‘Lloyd George’, but potentially inherited genes such as Ag₂ and Ag₃ or uncharacterized genes from ‘Cuthbert’ (Kennedy and Schaefers 1974). The development and deployment of molecular markers associated with each of these genes would be beneficial for breeders seeking to improve selection and combine multiple sources of resistance in future cultivars.